Proteomic responses to silver nanoparticles vary with the fungal ecotype

Enhanced commercial application of silver nanoparticles (AgNPs) is increasing the chance of their release into aquatic environments, potentially putting non-target microorganisms at risk. Impacts of AgNPs and Ag⁺ on two fungal ecotypes of Articulospora tetracladia, collected from a metal-polluted (At61) and a non-polluted (At72) stream, were assessed based on antioxidant enzymatic and proteomic responses. At61 showed more tolerance to AgNPs than At72 (EC₂₀, 158.9 vs 7.5 µg L^-1, respectively). Antioxidant enzyme activities were induced by AgNPs or Ag⁺ in both fungal ecotypes. Proteomic responses to AgNPs or Ag⁺ revealed that 41.3% of the total altered proteins were common in At72, while 27.3% were common in At61. In At72, gene ontology enrichment analyses indicated that Ag⁺ increased mainly the content of proteins involved in proteostasis and decreased the content of those related to vesicle-mediated transport; whereas the key group of proteins induced by AgNPs had functions in DNA repair and energy production. In At61, AgNPs induced proteins involved in energy production and protein biosynthesis, while both Ag forms induced proteins related to cell-redox and protein homeostasis, ascospore formation, fatty acid biosynthesis and nucleic acids metabolism. Both Ag forms induced stress-responsive proteins, and this was consistent with the responses of antioxidant enzymes. The negligible quantity of Ag⁺ released from AgNPs (<0.2 μg L^-1) supported a minor role of dissolved ionic form in AgNP-induced toxicity to both fungal ecotypes. Overall, results unraveled distinct mechanisms of toxicity and cellular targets of nanoparticulate and ionic silver in aquatic fungi with different environmental background, and constitutes a proof of concept that toxicants induce adaptive responses in microbes to face emergent contaminants.